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Received: 22 March 2017 Accepted: 14 August 2017 Published: xx xx xxxx
Riparian plant litter quality increases with latitude Luz Boyero1,2,3,4, Manuel A. S. Graça5, Alan M. Tonin6, Javier Pérez1, Andrew J. Swafford7, Verónica Ferreira5, Andrea Landeira-Dabarca5,8, Markos A. Alexandrou9, Mark O. Gessner10,11, Brendan G. McKie12, Ricardo J. Albariño13, Leon A. Barmuta14, Marcos Callisto15, Julián Chará16, Eric Chauvet17, Checo Colón-Gaud18, David Dudgeon19, Andrea C. Encalada5,20, Ricardo Figueroa21, Alexander S. Flecker22, Tadeusz Fleituch23, André Frainer24,25, José F. Gonçalves Jr.6, Julie E. Helson26, Tomoya Iwata27, Jude Mathooko28, Charles M’Erimba28, Catherine M. Pringle29, Alonso Ramírez30, Christopher M. Swan31, Catherine M. Yule32 & Richard G. Pearson3 Plant litter represents a major basal resource in streams, where its decomposition is partly regulated by litter traits. Litter-trait variation may determine the latitudinal gradient in decomposition in streams, which is mainly microbial in the tropics and detritivore-mediated at high latitudes. However, this hypothesis remains untested, as we lack information on large-scale trait variation for riparian litter. Variation cannot easily be inferred from existing leaf-trait databases, since nutrient resorption can cause traits of litter and green leaves to diverge. Here we present the first global-scale assessment of riparian litter quality by determining latitudinal variation (spanning 107°) in litter traits (nutrient 1
Faculty of Science and Technology, University of the Basque Country (UPV/EHU), Leioa, 48940, Spain. IKERBASQUE, Basque Foundation for Science, Bilbao, 48013, Spain. 3College of Science and Engineering, James Cook University, Townsville, 4811, QLD, Australia. 4Doñana Biological Station (EBD-CSIC), Sevilla, 41092, Spain. 5 MARE-Marine and Environmental Sciences Centre, Department of Life Sciences, University of Coimbra, PT-3001401, Coimbra, Portugal. 6Laboratorio de Limnologia/AquaRiparia, Departamento de Ecologia, IB, Universidade de Brasília, 70910-900, Brasília, Federal District, Brazil. 7Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, 93106, USA. 8Department of Ecology and Animal Biology, University of Vigo, 36330, Vigo, Spain. 9Wildlands Conservation Science, LLC, P.O. Box 1846, Lompoc, CA, 93438, USA. 10 Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), 16775, Stechlin, Germany. 11Department of Ecology, Berlin Institute of Technology (TU Berlin), 10587, Berlin, Germany. 12 Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, SE-75007, Uppsala, Sweden. 13Laboratorio de Fotobiología, INIBIOMA, CONICET, Universidad Nacional Comahue, Quintral 1250, 8400, Bariloche, Argentina. 14School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania, 7001, Australia. 15Laboratorio de Ecologia de Bentos, Departamento Biologia Geral, ICB, Universidade Federal de Minas Gerais, 30161-970, Belo Horizonte, MG, Brazil. 16Centro para la Investigación en Sistemas Sostenibles de Producción Agropecuaria (CIPAV), Carrera 25 No. 6-62, Cali, Colombia. 17EcoLab, Université de Toulouse, CNRS, INP, UPS, 118 Route de Narbonne, 31062, Toulouse, France. 18Department of Biology, Georgia Southern University, Statesboro, Georgia, 30458, USA. 19School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong, SAR, China. 20Laboratorio de Ecología Acuática, Colegio de Ciencias Biológicas y Ambientales, Universidad San Francisco de Quito, Campus Cumbayá, P.O. Box 17, 1200 841, Quito, Ecuador. 21Facultad de Ciencias Ambientales y Centro de Recursos Hidricos para la Agricultura y la Minería, Universidad de Concepción, Concepción, Chile. 22 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA. 23Institute of Nature Conservation, Polish Academy of Sciences, Mickiewicza 33, 31-120, Kraków, Poland. 24Department of Ecology and Environmental Science, Umeå University, Umeå, Sweden. 25Department of Arctic and Marine Biology, UiT The Arctic University of Norway, 9037, Tromsø, Norway. 26Surface and Groundwater Ecology Research Group, Department of Biological Sciences, University of Toronto at Scarborough, 1265 Military Trail, Toronto, Ontario, M1C 1A4, Canada. 27Department of Environmental Sciences, University of Yamanashi, Kofu, Yamanashi, 400-8510, Japan. 28 Department of Biological Sciences, Egerton University, PO Box 536, Egerton, Kenya. 29Odum School of Ecology, University of Georgia, 30602, Athens, GA, USA. 30Department of Environmental Science, University of Puerto Rico, Río Piedras, San Juan, Puerto Rico, 00919, USA. 31Department of Geography and Environmental Systems, University of Maryland, Baltimore County, Baltimore, MD, 21250, USA. 32School of Science, Monash University, Jalan Lagoon Selatan, Bandar Sunway, Selangor, 47500, Malaysia. Correspondence and requests for materials should be addressed to L.B. (email:
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SCIENTIFIC RePorTs | 7: 10562 | DOI:10.1038/s41598-017-10640-3
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www.nature.com/scientificreports/ concentrations; physical and chemical defences) of 151 species from 24 regions and their relationships with environmental factors and phylogeny. We hypothesized that litter quality would increase with latitude (despite variation within regions) and traits would be correlated to produce ‘syndromes’ resulting from phylogeny and environmental variation. We found lower litter quality and higher nitrogen:phosphorus ratios in the tropics. Traits were linked but showed no phylogenetic signal, suggesting that syndromes were environmentally determined. Poorer litter quality and greater phosphorus limitation towards the equator may restrict detritivore-mediated decomposition, contributing to the predominance of microbial decomposers in tropical streams. About 90% of the plant material produced annually in terrestrial ecosystems escapes herbivory and enters the pool of dead organic matter1, 2. Some of this plant litter is stored in soils and sediments over long periods, but much of it is decomposed, often providing a key basal resource for food webs in both terrestrial and aquatic ecosystems3–5. Ultimately, the fate of this organic matter influences the global carbon cycle through the release or sequestration of carbon dioxide (CO2) and other greenhouse gasses6. Stream ecosystems contribute significantly to CO2 release7, with a substantial proportion of the emitted CO2 being derived from in-stream biological activity8. In these systems, plant litter comes from the surrounding riparian vegetation, and it is decomposed by invertebrate detritivores and microorganisms9. However, the relative role of these decomposers changes across large spatial scales, including latitudinal gradients. While litter-consuming detritivores play a fundamental role in streams at mid and high latitudes, decomposition near the equator is mainly due to microbes10. Understanding the factors driving this latitudinal gradient is important because changes in the relative role of microbial decomposers and detritivores lead to differences in the amount of CO2 produced in different regions of the planet, and understanding this spatial variation may help forecast future emissions10. Large-scale patterns of detritivore abundance and diversity are probably important determinants of the latitudinal decomposition gradient: litter-consuming detritivores are scarcer and less diverse in many tropical areas11, possibly as a result of elevated temperatures that are unfavourable to detritivores (many of which are cool-adapted taxa)12 and the reduced dispersal abilities of tropical detritivores13. However, it has also been proposed that differences in decomposition rate across latitudes are influenced by changes in the characteristics of riparian plant litter14. There is much evidence that litter traits affect decomposition rates in streams: in particular, decomposition is reduced when concentrations of lignin15, 16 or tannins17 are high or when litter is particularly tough18 and is often reported to be enhanced when litter nutrient concentrations are high19, 20. Similar relationships have been found for litter decomposition in terrestrial ecosystems21–24. It is unknown, however, whether riparian litter traits change systematically along latitudinal gradients, and comparative information for terrestrial plant litter is also scarce at the global scale. This contrasts with the large number of comparative studies on green leaves, which have been mostly motivated by an interest in plant-herbivore interactions, following Dobzhansky25. Green leaves are typically poorer in nutrients in the tropics than at higher latitudes26, 27, and possibly better defended against herbivory1, 2 (but see ref. 28). However, the very few studies that have explored litter traits globally have found that traits of litter can differ from those of green leaves29, partly because of differences in nutrient resorption efficiency across latitudes30. This highlights the importance of quantifying trait variation of litter, rather than assuming that patterns for green leaves also pertain to litter. The most comprehensive study of litter trait variation, which used a dataset of 638 plant species across 6 biomes, showed that litter from tropical forests had higher nitrogen (N) but lower phosphorus (P) than litter from other biomes30. The other two existing global studies examined a wider range of traits, but included a limited number of species. This includes a study of 16 plant species from 4 biomes reporting higher lignin and hemicellulose concentrations in tropical litter, higher N concentration in temperate litter, higher concentrations of phenols and tannins in Mediterranean litter, and higher concentrations of P and micronutrients such as magnesium (Mg) and calcium (Ca) in subarctic litter23. The other study, involving a total of 20 plant species from 5 biomes, found that tropical litter was tougher, had lower specific leaf area (SLA) and lower concentrations of Mg and Ca than litter from other biomes19. Here we present the first comprehensive study assessing riparian litter quality at the global scale, encompassing 151 riparian plant species (Supplementary Table S1) from 24 sites on six continents, spanning 107° of latitude and a wide climatic gradient (Supplementary Table S2), and multiple litter traits relevant for decomposition. We explored latitudinal variation in the concentration of major nutrients (N, P and their ratio, and Mg), physical defences (SLA, used as an inverse proxy for toughness) and chemical defences (concentration of condensed tannins), and the influence of climatic factors and soil characteristics in determining patterns of variation. We also explored how traits might be linked in ‘trait syndromes’31 (for example, litter with high nutrient concentrations might also be associated with low concentrations of tannins and low toughness, resulting in overall high litter quality; or vice versa), and whether such syndromes might be determined by environmental drivers or species’ phylogenetic relatedness. We predicted that (i) litter trait variation would be closely related to gradients in precipitation and temperature (and hence latitude), with litter quality decreasing towards the equator, (ii) significant variation would also occur within climatic regions due to local climatic gradients (e.g., in relation to altitude and soil characteristics), and (iii) traits would be linked in high- or low-quality syndromes mostly determined by environmental drivers, but with an influence of phylogeny also apparent.
Results
The two first axes of the Principal Component Analysis (PCA) explained 47.1% of the variance in litter traits and environmental variables (Fig. 1). The first axis (31.9%) was mostly related to latitude and temperature [both mean annual temperature (MAT) and temperature seasonality (TS)], with the tropical and non-tropical samples SCIENTIFIC RePorTs | 7: 10562 | DOI:10.1038/s41598-017-10640-3
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Figure 1. Principal component analysis (PCA) of litter traits [nitrogen (N) and phosphorus (P) concentration, N:P ratio, magnesium (Mg) and tannin (Tan) concentration, and specific leaf area (SLA); in bold letters] and environmental and spatial variables (mean annual temperature, MAT; mean annual precipitation, MAP; precipitation of the driest quarter, PDQ; temperature seasonality, TS; precipitation seasonality, PS; latitude, Lat; and altitude, Alt). Open and closed circles represent species from tropical and non-tropical regions (i.e., temperate, Mediterranean and boreal), respectively.
almost completely separated; the litter traits related to this axis were the N:P ratio (which increased with MAT and decreased with latitude and TS) and SLA, which showed the opposite pattern. The second axis (15.2%) was mostly related to altitude, precipitation of the driest quarter (PDQ), and two soil characteristics [pH and organic content (OC)]; the litter traits related to this axis were N and P concentrations and SLA (all inversely related to altitude and aridity). Tannins showed weak relationships with both axes, increasing towards lower latitudes and higher altitudes, and Mg showed a weak relationship with the first axis, increasing with latitude. Linear models explained 14–37% of the global variation in litter traits, and showed strong relationships between different traits (Table 1, Fig. 2). In particular, N and P concentrations were highly related, tannin concentration was tightly related to N and Mg concentrations, and a significant fraction of SLA variation was associated with tannin and P concentration. The most important environmental predictor for N concentration was mean annual precipitation (MAP; modulated by MAT), with some influence of soil pH; P concentration was associated with MAT, soil N concentration and soil pH; N:P was mostly related to MAT, modulated by MAP; Mg was correlated with soil N, MAP and soil pH; tannins were related to MAP, MAT and soil pH; and SLA was associated with MAT and soil N. Most traits showed significant latitudinal variation (Fig. 2): N concentration showed a significant (p = 0.002), nonlinear trend, being intermediate at low latitudes, decreasing at mid latitudes (≈20–40°) and increasing towards higher latitudes; an apparent curvilinear trend in P concentration was not significant (p = 0.064); the N:P ratio showed a significant linear trend (p = 0.006), decreasing with latitude; tannin concentration also decreased with latitude (p = 0.016); SLA strongly increased with latitude (p
